Frequency-independent synaptic transmission supports a linear vestibular behavior.
The vestibular system is responsible for transforming head motion into precise eye, head, and body movements that rapidly stabilize gaze and posture. How do central excitatory synapses mediate behavioral outputs accurately matched to sensory inputs over a wide dynamic range? Here we demonstrate that vestibular afferent synapses in vitro express frequency-independent transmission that spans their in vivo dynamic range (5-150 spikes/s). As a result, the synaptic charge transfer per unit time is linearly related to vestibular afferent activity in both projection and intrinsic neurons of the vestibular nuclei. Neither postsynaptic glutamate receptor desensitization nor saturation affect the relative amplitude or frequency-independence of steady-state transmission. Finally, we show that vestibular nucleus neurons can transduce synaptic inputs into linear changes in firing rate output without relying on one-to-one calyceal transmission. These data provide a physiological basis for the remarkable linearity of vestibular reflexes.
Bagnall
Martha W
MW
Neurosciences Graduate Program, University of California San Diego, San Diego, CA 92093, USA.
McElvain
Lauren E
LE
Faulstich
Michael
M
du Lac
Sascha
S
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D007395:Interneurons / Q000166:cytology / Q000502:physiology; D016014:Linear Models; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009924:Organ Culture Techniques; D018408:Patch-Clamp Techniques; D004856:Postural Balance / Q000502:physiology*; D017470:Receptors, Glutamate / Q000502:physiology; D012027:Reflex, Vestibulo-Ocular / Q000502:physiology*; D011984:Sensory Receptor Cells / Q000166:cytology / Q000502:physiology*; D013569:Synapses / Q000502:physiology* / Q000648:ultrastructure; D009435:Synaptic Transmission / Q000502:physiology*; D014725:Vestibular Nerve / Q000502:physiology; D014726:Vestibular Nuclei / Q000166:cytology / Q000502:physiology*; D014722:Vestibule, Labyrinth / Q000502:physiology
D017470:Receptors, Glutamate